A test for the genetic basis of natural selection: an individual-based longitudinal study in a stream-dwelling fish

In addition to the well-studied evolutionary parameters of (1) phenotype-fitness covariance and (2) the genetic basis of phenotypic variation, adaptive evolution by natural selection requires that (3) fitness variation is effected by heritable genetic differences among individuals and (4) phenotype-fitness covariances must be, at least in part, underlain by genetic covariances. These latter two requirements for adaptive evolutionary change are relatively unstudied in natural populations. Absence of the latter requirements could explain stasis of apparently directionally selected heritable traits. We provide complementary analyses of selection and variation at phenotypic and genetic levels for juvenile growth rate in brook charr Salvelinus fontinalis in Freshwater River, Newfoundland, Canada. Contrary to the vast majority of reports in fish, we found very little viability selection of juvenile body size. Large body size appears nonetheless to be selectively advantageous via a relationship with early maturity. Genetic patterns in evolutionary parameters largely reflected phenotypic patterns. We have provided inference of selection based on longitudinal data, which are uncommon in high fecundity organisms. Furthermore we have provided a practicable framework for further studies of the genetic basis of natural selection.     

Origin of evolutionary novelty: examples from limbs

Classic hypotheses of vertebrate morphology are being informed by new data and new methods. Long nascent issues, such as the origin of tetrapod limbs, are being explored by paleontologists, molecular biologists, and functional anatomists. Progress in this arena will ultimately come down to knowing how macroevolutionary differences between taxa emerge from the genetic and phenotypic variation that arises within populations. The assembly of limbs over developmental and evolutionary time offers examples of the major processes at work in the origin of novelties. Recent comparative developmental analyses demonstrate that many of the mechanisms used to pattern limbs are ancient. One of the major consequences of this phenomenon is parallelism in the evolution of anatomical structures. Studies of both the fossil record and intrapopulational variation of extant populations reveal regularities in the origin of variation. These examples reveal processes acting at the level of populations that directly affect the patterns of diversity observed at higher taxonomic levels.     

Liberating genetic variance through sex

Genetic variation in fitness is the fundamental prerequisite for adaptive evolutionary change. If there is no variation in survival and reproduction or if this variation has no genetic basis, then the composition of a population will not evolve over time. Consequently, the factors influencing genetic variation in fitness have received close attention from evolutionary biologists. One key factor is the mode of reproduction. Indeed, it has long been thought that sex enhances fitness variation and that this explains the ubiquity of sexual reproduction among eukaryotes. Nevertheless, theoretical studies have demonstrated that sex need not always increase genetic variation in fitness. In particular, if fitness interactions among beneficial alleles (epistasis) are positive, sex can reduce genetic variance in fitness. Empirical data have been sorely needed to settle the issue of whether sex does enhance fitness variation. A recent flurry of studies[1-4] has demonstrated that sex and recombination do dramatically increase genetic variation in fitness and consequently the rate of adaptive evolution. Interpreted in light of evolutionary theory, these studies rule out positive in these experiments epistasis as a major source of genetic associations. Further studies are needed, however, to tease apart other possible sources.     

What is wrong with absolute individual fitness?

One of the most basic facts about evolution is that fitness is a relative concept. It does not matter how well an organism survives and reproduces, only that it does so better than other organisms bearing alternative traits. Nevertheless, many evolutionary arguments are framed in terms of absolute individual fitness. The absolute fitness criterion (AFC) can be justified in terms of relative fitness only given certain assumptions that are frequently violated in nature. In particular, interactions must occur in groups that are randomly formed and phenotypic variation among groups must be tightly coupled to genetic variation. Complicating the genotype-phenotype relationship can cause phenotypic variation among groups to become nonrandom, even when the groups are randomly formed, favoring traits that do not maximize absolute individual fitness. Complex genotype-phenotype relationships and complex population structures require explicit models of evolutionary change based on relative fitness differences within and among groups.     

Neutral mutation as the source of genetic variation in life history traits

The mechanism underlying the maintenance of adaptive genetic variation is a long-standing question in evolutionary genetics. There are two concepts (mutation-selection balance and balancing selection) which are based on the phenotypic differences between alleles. Mutation - selection balance and balancing selection cannot properly explain the process of gene substitution, i.e. the molecular evolution of quantitative trait loci affecting fitness. I assume that such loci have non-essential functions (small effects on fitness), and that they have the potential to evolve into new functions and acquire new adaptations. Here I show that a high amount of neutral polymorphism at these loci can exist in real populations. Consistent with this, I propose a hypothesis for the maintenance of genetic variation in life history traits which can be efficient for the fixation of alleles with very small selective advantage. The hypothesis is based on neutral polymorphism at quantitative trait loci and both neutral and adaptive gene substitutions. The model of neutral - adaptive conversion (NAC) assumes that neutral alleles are not neutral indefinitely, and that in specific and very rare situations phenotypic (relative fitness) differences between them can appear. In this paper I focus on NAC due to phenotypic plasticity of neutral alleles. The important evolutionary consequence of NAC could be the increased adaptive potential of a population. Loci responsible for adaptation should be fast evolving genes with minimally discernible phenotypic effects, and the recent discovery of genes with such characteristics implicates them as suitable candidates for loci involved in adaptation.     

Adapting to winter in wheat: a long-term study follows parallel phenotypic and genetic changes in three experimental wheat populations

Drawing a direct connection between adaptive evolution at the phenotypic level and underlying genetic factors has long been a major goal of evolutionary biologists, but the genetic characterization of adaptive traits in natural populations is notoriously difficult. The study of evolution in experimental populations offers some help — initial conditions are known and changes can be tracked for extended periods under conditions more controlled than wild populations and more realistic than laboratory or greenhouse experiments. In this issue of Molecular Ecology , researchers studying experimental wheat populations over a 12-year period have demonstrated evolution in a major adaptive trait, flowering time, and parallel changes in underlying genetic variation ( Rhoné et al . 2008 ). Their work suggests that cis -regulatory mutations at a single gene may explain most of the flowering time variation in these populations.     

Developmental processes regulate craniofacial variation in disease and evolution

Variation in development mediates phenotypic differences observed in evolution and disease. Although the mechanisms underlying phenotypic variation are still largely unknown, recent research suggests that variation in developmental processes may play a key role. Developmental processes mediate genotype–phenotype relationships and consequently play an important role regulating phenotypes. In this review, we provide an example of how shared and interacting developmental processes may explain convergence of phenotypes in spliceosomopathies and ribosomopathies. These data also suggest a shared pathway to disease treatment. We then discuss three major mechanisms that contribute to variation in developmental processes: genetic background (gene–gene interactions), gene–environment interactions, and developmental stochasticity. Finally, we comment on evolutionary alterations to developmental processes, and the evolution of disease buffering mechanisms.     

Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.     

No selection for change in polyandry under experimental evolution

What drives mating system variation is a major question in evolutionary biology. Female multiple mating (polyandry) has diverse evolutionary consequences, and there are many potential benefits and costs of polyandry. However, our understanding of its evolution is biased towards studies enforcing monandry in polyandrous species. What drives and maintains variation in polyandry between individuals, genotypes, populations and species remains poorly understood. Genetic variation in polyandry may be actively maintained by selection, or arise by chance if polyandry is selectively neutral. In Drosophila pseudoobscura, there is genetic variation in polyandry between and within populations. We used isofemale lines to found replicate populations with high or low initial levels of polyandry and tracked polyandry under experimental evolution over seven generations. Polyandry remained relatively stable, reflecting the starting frequencies of the experimental populations. There were no clear fitness differences between high versus low polyandry genotypes, and there was no signature of balancing selection. We confirmed these patterns in direct comparisons between evolved and ancestral females and found no consequences of polyandry for female fecundity. The absence of differential selection even when initiating populations with major differences in polyandry casts some doubt on the importance of polyandry for female fitness.     

Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in <Emphasis Type="Italic">Arabidopsis thaliana</Emphasis>

Heritable phenotypic variation in plants can be caused not only by underlying genetic differences, but also by variation in epigenetic modifications such as DNA methylation. However, we still know very little about how relevant such epigenetic variation is to the ecology and evolution of natural populations. We conducted a greenhouse experiment in which we treated a set of natural genotypes of Arabidopsis thaliana with the demethylating agent 5-azacytidine and examined the consequences of this treatment for plant traits and their phenotypic plasticity. Experimental demethylation strongly reduced the growth and fitness of plants and delayed their flowering, but the degree of this response varied significantly among genotypes. Differences in genotypes’ responses to demethylation were only weakly related to their genetic relatedness, which is consistent with the idea that natural epigenetic variation is independent of genetic variation. Demethylation also altered patterns of phenotypic plasticity, as well as the amount of phenotypic variation observed among plant individuals and genotype means. We have demonstrated that epigenetic variation can have a dramatic impact on ecologically important plant traits and their variability, as well as on the fitness of plants and their ecological interactions. Epigenetic variation may thus be an overlooked factor in the evolutionary ecology of plant populations.     

Molecular and morphometric variation in chromosomally differentiated populations of the grasshopper Sinipta dalmani (Orthopthera: Acrididae)

Sinipta dalmani is an Argentine grasshopper whose chromosome polymorphisms have been widely studied through cytogenetic, morphometric, and fitness component analyses. The present work analysed molecular and morphometric variation in seven chromosomally differentiated populations from Entre Rios and Buenos Aires provinces to analyse population structure. Molecular studies were performed studying RAPD loci and morphometric analyses were carried out measuring five morphometric traits. Genetic variability was high in all studied populations and was characterized by a decrease in H as a function of latitude and temperature. Both conventional F(ST) analysis and Bayesian approach for dominant marker showed that there were significant genetic differences among all populations, between provinces, and among populations within provinces. Entre Rios populations showed higher mean numbers of migrants per generation as well as low genetic differentiation and high gene flow with almost all populations whereas Buenos Aires populations may be considered as a result of a more recently colonization. There is considerable morphometric variation between populations and this variation correlates with latitude and temperature. Our results suggest that selection contributes to phenotypic differentiation among populations by moulding the differences in trait means whereas genetic drift is responsible for differences in the matrix of variance-covariance. The gene flow detected is insufficient to prevent phenotypic and chromosome divergences.     

Genetic Diversity and the Survival of Populations

Abstract: In this comprehensive review, a range of factors is considered that may influence the significance of genetic diversity for the survival of a population. Genetic variation is essential for the adaptability of a population in which quantitatively inherited, fitness-related traits are crucial. Therefore, the relationship between genetic diversity and fitness should be studied in order to make predictions on the importance of genetic diversity for a specific population. The level of genetic diversity found in a population highly depends on the mating system, the evolutionary history of a species and the population history (the latter is usually unknown), and on the level of environmental heterogeneity. An accurate estimation of fitness remains complex, despite the availability of a range of direct and indirect fitness parameters. There is no general relationship between genetic diversity and various fitness components. However, if a lower level of heterozygosity represents an increased level of inbreeding, a reduction in fitness can be expected. Molecular markers can be used to study adaptability or fitness, provided that they represent a quantitative trait locus (QTL) or are themselves functional genes involved in these processes. Next to a genetic response of a population to environmental change, phenotypic plasticity in a genotype can affect fitness. The relative importance of plasticity to genetic diversity depends on the species and population under study and on the environmental conditions. The possibilities for application of current knowledge on genetic diversity and population survival for the management of natural populations are discussed.     

Phenotypic plasticity and selection in Drosophila life history evolution. 2. Diet,mates and the cost of reproduction

While it is commonplace for biologists to use the response to environmental manipulation as a guide to evolutionary responses to selection, the relationship between phenotypic plasticity and genetic change is not generally well-established. The life-histories of laboratory Drosophila populations are among the few experimental systems which simultaneously afford information on phenotypic plasticity and evolutionary trajectories. We employed a combination of two replicated selectively differentiated stocks (postponed aging stocks and their controls; 10 populations in total) and two different environmental manipulations (nutrition and mating) to explore the empirical relationship between phenotypic plasticity and evolutionary trajectories. While there are a number of parallels between the results obtained using these two approaches, there are important differences. In particular, as the detail of the biological characterization of either type of response increases, so their disparities multiply. Nonetheless, the combination of environmental manipulation with evolutionary divergence provides valuable information about the biological connections between life-history, caloric reserves, and reproductive physiology in Drososphila.     

The evolution of the phenotypic covariance matrix: evidence for selection and drift in Melanoplus

Phenotypic variation in trait means is a common observation for geographically separated populations. Such variation is typically retained under common garden conditions, indicating that there has been evolutionary change in the populations, as a result of selection and/or drift. Much less frequently studied is variation in the phenotypic covariance matrix (hereafter, P matrix), although this is an important component of evolutionary change. In this paper, we examine variation in the phenotypic means and P matrices in two species of grasshopper, Melanoplus sanguinipes and M. devastator. Using the P matrices estimated for 14 populations of M. sanguinipes and three populations of M. devastator we find that (1) significant differences between the sexes can be attributed to scaling effects; (2) there is no significant difference between the two species; (3) there are highly significant differences among populations that cannot be accounted for by scaling effects; (4) these differences are a consequence of statistically significant patterns of covariation with geographic and environmental factors, phenotypic variances and covariances increasing with increased temperature but decreasing with increased latitude and altitude. This covariation suggests that selection has been important in the evolution of the P matrix in these populations Finally, we find a significant positive correlation between the average difference between matrices and the genetic distance between the populations, indicating that drift has caused some of the variation in the P matrices.     

RESPONSE TO NATURAL ENVIRONMENTAL HETEROGENEITY: MATERNAL EFFECTS AND SELECTION ON LIFE-HISTORY CHARACTERS AND PLASTICITIES IN MIMULUS GUTTATUS

Recent studies in plant populations have found that environmental heterogeneity and phenotypic selection vary at local spatial scales. In this study, I ask if there is evolutionary change in response to environmental heterogeneity and, if so, whether the response occurs for characters or character plasticities. I used vegetative clones of Mimulus guttatus to create replicate populations of 75 genotypes. These populations were planted into the natural habitat where they differed in mean growth, flowering phenology, and life span. This phenotypic variation was used to define selective environments. There was variation in fitness (flower production) among genotypes across all planting sites and in genotype response to the selective environment. Offspring from each site were grown in the greenhouse in two water treatments. Because each population initially had the same genetic composition, variation in the progeny between selective environments reveals either evolutionary change in response to environmental heterogeneity or environmental maternal effects. Plants from experimental sites that flowered earlier, had shorter life spans and were less productive, produced offspring that had more flowers, on average, and were less plastic in vegetative allocation than offspring of longer-lived plants from high-productivity areas. However, environmental maternal effects masked phenotypic differences in flower production. Therefore, although there was evidence of genetic differentiation in both life-history characters and their plasticities in response to small-scale environmental heterogeneity, environmental maternal effects may slow evolutionary change. Response to local-scale selective regimes suggests that environmental heterogeneity and local variation in phenotypic selection may act to maintain genetic variation.     

Molecular ecological approaches to studying the evolutionary impact of selective harvesting in wildlife

Harvesting of wildlife populations by humans is usually targeted by sex, age or phenotypic criteria, and is therefore selective. Selective harvesting has the potential to elicit a genetic response from the target populations in several ways. First, selective harvesting may affect population demographic structure (age structure, sex ratio), which in turn may have consequences for effective population size and hence genetic diversity. Second, wildlife-harvesting regimes that use selective criteria based on phenotypic characteristics (e.g. minimum body size, horn length or antler size) have the potential to impose artificial selection on harvested populations. If there is heritable genetic variation for the target characteristic and harvesting occurs before the age of maturity, then an evolutionary response over time may ensue. Molecular ecological techniques offer ways to predict and detect genetic change in harvested populations, and therefore have great utility for effective wildlife management. Molecular markers can be used to assess the genetic structure of wildlife populations, and thereby assist in the prediction of genetic impacts by delineating evolutionarily meaningful management units. Genetic markers can be used for monitoring genetic diversity and changes in effective population size and breeding systems. Tracking evolutionary change at the phenotypic level in the wild through quantitative genetic analysis can be made possible by genetically determined pedigrees. Finally, advances in genome sequencing and bioinformatics offer the opportunity to study the molecular basis of phenotypic variation through trait mapping and candidate gene approaches. With this understanding, it could be possible to monitor the selective impacts of harvesting at a molecular level in the future. Effective wildlife management practice needs to consider more than the direct impact of harvesting on population dynamics. Programs that utilize molecular genetic tools will be better positioned to assess the long-term evolutionary impact of artificial selection on the evolutionary trajectory and viability of harvested populations.     

Strong artificial selection in the wild results in predicted small evolutionary change

Estimates of genetic variation and selection allow for quantitative predictions of evolutionary change, at least in controlled laboratory experiments. Natural populations are, however, different in many ways, and natural selection on heritable traits does not always result in phenotypic change. To test whether we were able to predict the evolutionary dynamics of a complex trait measured in a natural, heterogeneous environment, we performed, over an 8-year period, a two-way selection experiment on clutch size in a subdivided island population of great tits (Parus major). Despite strong artificial selection, there was no clear evidence for evolutionary change at the phenotypic level. Environmentally induced differences in clutch size among years are, however, large and can mask evolutionary changes. Indeed, genetic changes in clutch size, inferred from a statistical model, did not deviate systematically from those predicted. Although this shows that estimates of genetic variation and selection can indeed provide quantitative predictions of evolutionary change, also in the wild, it also emphasizes that demonstrating evolution in wild populations is difficult, and that the interpretation of phenotypic trends requires great care.